Coevolutionary relationship between striatum size and social play in nonhuman primates

The striatum is a region of the brain specifically tied to the experience and anticipation of pleasure, reward, appropriate behavioral sequencing, cognition, learning, and social modulation. Furthermore, the striatum is connected neurologically and functionally to other brain regions associated with the exhibition of social play, such as the neocortex, cerebellum, and limbic system. For these reasons, the striatum is especially interesting to researchers of play behavior. Moreover, the caudate-putamen area of the striatum has been specifically implicated in laboratory studies of social play behavior. This study uses the phylogenetic comparative method of independent contrasts to test for an evolutionary relationship between striatum volume and a measure of social play in nonhuman primates. Relative volume of the primate striatum correlates with rate of social, but not nonsocial, play behavior across species, suggesting a coevolution of traits. The pleasurable and procedural aspects of social play behavior may be mediated in part by the striatum and further to its connection to dopaminergic pathways in the primate brain.     

Abnormal births and other “ill omens”

We summarize the ethnographic literature illustrating that “abnormal birth” circumstances and “ill omens” operate as cues to terminate parental investment. A review of the medical literature provides evidence to support our assertion that ill omens serve as markers of biological conditions that will threaten the survival of infants. Daly and Wilson (1984) tested the prediction that children of demonstrably poor phenotypic quality will be common victims of infanticide. We take this hypothesis one stage further and argue that some children will be poor vehicles for parental investment yet are not of demonstrably poor quality at birth. We conclude that when people dispose of infants due to “superstitious beliefs” they are pursuing an adaptive strategy in eliminating infants who are poor vehicles for parental investment. Catherine Hill lectures in biological anthropology/human sciences at Durham University’s University College, Stockton. She trained in biological anthropology at University College, London. Her current research interests include human and nonhuman primate socioecology and human resource ecology and development issues. Helen Ball lectures in biological anthropology/human sciences at Durham University’s University College, Stockton. She trained in biological anthropology at the University of Massachusetts at Amherst. Her current research interests include nonhuman primate behavior and socioecology, reproductive biology, and evolutionary issues.     

Dramatic increases in number of cerebellar granule-cell-Purkinje-cell synapses across several mammals

The classical comparative literature on mammalian brain evolution has mainly focused on brain mass measurements because larger brains are more likely to have more neurons to process information. The phylogenetic expansion in the mass of the cerebellum is as significant as that of the cerebral cortex. The synapse, however, has recently been recognized as the basic unit of neuronal information processing, including neuroplasticity. Here we hypothesize significant absolute and relative increases in the functionally important granule-cell-Purkinje-cell (gcPc) synapses as a salient feature of the evolving cerebellum. To probe evolutionary constraints, we define the gcPc circuitry with ten degrees of freedom, including number of granule cells, Purkinje cells, lengths of the granule cell axonal segments, linear densities of synapses along them, and physical dimensions of Purkinje as well as granule cell dendritic structures. We show that although only two of the ten parameters are not constrained and therefore can exhibit independent, comparative changes, there is a dramatic increase in the number of gcPc synapses from the rodent to the human cerebellum. By assigning a value of unity for the mouse, the ratio of the number of gcPc synapses from mouse, rat, cat, non-human primate, and human is 1:5.5:236:620:20,000, which greatly exceeds the ratio of increase in cerebellar mass (1:6:48:180:3000). Dramatic changes in the number of gcPc synapses can therefore occur despite evolutionary constraints and only modest changes in parameters of the neuronal circuitry. Increases in the number of gcPc synapses have important functional consequences as these synapses enhance the capacity of the cerebellum to code and process information, which directly impact memory and learning in both motor and non-motor tasks.     

The Use (and Misuse) of Phylogenetic Trees in Comparative Behavioral Analyses

Phylogenetic comparative methods play a critical role in our understanding of the adaptive origin of primate behaviors. To incorporate evolutionary history directly into comparative behavioral research, behavioral ecologists rely on strong, well-resolved phylogenetic trees. Phylogenies provide the framework on which behaviors can be compared and homologies can be distinguished from similarities due to convergent or parallel evolution. Phylogenetic reconstructions are also of critical importance when inferring the ancestral state of behavioral patterns and when suggesting the evolutionary changes that behavior has undergone. Improvements in genome sequencing technologies have increased the amount of data available to researchers. Recently, several primate phylogenetic studies have used multiple loci to produce robust phylogenetic trees that include hundreds of primate species. These trees are now commonly used in comparative analyses and there is a perception that we have a complete picture of the primate tree. But how confident can we be in those phylogenies? And how reliable are comparative analyses based on such trees? Herein, we argue that even recent molecular phylogenies should be treated cautiously because they rely on many assumptions and have many shortcomings. Most phylogenetic studies do not model gene tree diversity and can produce misleading results, such as strong support for an incorrect species tree, especially in the case of rapid and recent radiations. We discuss implications that incorrect phylogenies can have for reconstructing the evolution of primate behaviors and we urge primatologists to be aware of the current limitations of phylogenetic reconstructions when applying phylogenetic comparative methods.     

D'scent of man: A comparative survey of primate chemosignaling in relation to sex

This article is part of a Special Issue (Chemosignals and Reproduction).As highly visual animals, primates, in general, and Old World species (including humans), in particular, are not immediately recognized for reliance in their daily interactions on olfactory communication. Nevertheless, views on primate olfactory acuity and the pervasiveness of their scent signaling are changing, with increased appreciation for the important role of body odors in primate social and sexual behavior. All major taxonomic groups, from lemurs to humans, are endowed with scent-producing organs, and either deposit or exude a wealth of volatile compounds, many of which are known semiochemicals. This review takes a comparative perspective to illustrate the reproductive context of primate signaling, the relevant information content of their signals, the sexually differentiated investigative responses generated, and the behavioral or physiological consequences of message transmission to both signaler and receiver. Throughout, humans are placed alongside their relatives to illustrate the evolutionary continuum in the sexual selection of primate chemosignals. This ever-growing body of evidence points to a critical role of scent in guiding the social behavior and reproductive function throughout the primate order.     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Brain levels of arginine-vasotocin and isotocin in dominant and subordinate males of a cichlid fish

The nonapeptides arginine-vasotocin (AVT) and isotocin (IT), which are the teleost homologues of arginine-vasopressin and oxytocin in mammals, have well established peripheral effects on osmoregulation and stress response, and central effects on social behavior. However, all studies that have looked so far into the relationship between these nonapeptides and social behavior have used indirect measures of AVT/IT activity (i.e. immunohistochemistry of AVT/IT immunoreactive neurons, or AVT/IT or their receptors mRNA expression with in situ hybridization or qPCR) and therefore direct measures of peptide levels in relation to social behavior are still lacking. Here we use a recently developed high-performance liquid chromatography analysis with fluorescence detection (HPLC-FL) method to quantify the levels of both AVT and IT in macro-dissected brain areas [i.e. olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and hindbrain (= rhombencephalon minus cerebellum)] and pituitary of dominant and subordinate male cichlid fish (Oreochromis mossambicus). The pituitary shows higher levels of both peptides than any of the brain macroareas, and the olfactory bulbs have the highest AVT among all brain areas. Except for IT in the telencephalon there is a lack of correlations between central levels and pituitary peptide levels, suggesting an independent control of hypophysial and CNS nonapeptide secretion. There were also no correlations between AVT and IT levels either for each brain region or for the pituitary gland, suggesting a decoupled activity of the AVT and IT systems at the CNS level. Subordinate AVT pituitary levels are significantly higher than those of dominants, and dominant hindbrain IT levels are significantly higher than those of subordinates, suggesting a potential involvement of AVT in social stress in subordinate fish and of IT in the regulation of dominant behavior at the level of the hindbrain. Since in this species dominant males use urine to communicate social status and since AVT is known to have an antidiuretic effect, we have also investigated the effect of social status on urine storage. As predicted, dominant males stored significantly more urine than subordinates. Given these results we suggest that AVT/IT play a key role in orchestrating social phenotypes, acting both as central neuromodulators that promote behavioral plasticity and as peripheral hormones that promote integrated physiological changes.     

Females drive primate social evolution

Within and across species of primates, the number of males in primate groups is correlated with the number of females. This correlation may arise owing to ecological forces operating on females, with subsequent competition among males for access to groups of females. The temporal relationship between changes in male and female group membership remains unexplored in primates and other mammalian groups. We used a phylogenetic comparative method for detecting evolutionary lag to test whether evolutionary change in the number of males lags behind change in the number of females. We found that change in male membership in primate groups is positively correlated with divergence time in pairwise comparisons. This result is consistent with male numbers adjusting to female group size and highlights the importance of focusing on females when studying primate social evolution.     

Assessing variation in the social behavior of stumptail macaques using thermal criteria

This paper reports a method for comparing the environments of nonhuman primates based on biophysical, thermal criteria. The method is applied to an analysis of behaviors exhibited by group-living stumptail macaques (Macaca arctoides), documented by a group-scan observation technique, to test the hypothesis that the expression of social behavior is dependent on thermal conditions. Thermal conditions are identified by considering sky cover and the relative cooling power of the environment. The results show that the rates of occurrence of affiliative, play, and solitary behaviors are altered significantly at a relative cooling power at or above 550 kcal/m2/hr under cloudy conditions and at or above 600 kcal/m2/hr under sunny conditions. In addition, the rates of occurrence of play, sexual, aggressive, and submissive behavioral states are also significantly different under cloudy, rather than sunny, conditions over particular ranges of cooling. It is possible to conclude that thermal criteria affect the expression of social behaviors by stumptail macaques. This is consistent with studies of huddling behavior exhibited by stumptail macaques and rhesus macaques (M. mulatta), and suggests that 1) certain changes in the expression of social behaviors may be thermoregulatory in at least some nonhuman primate species and 2) thermal criteria are likely to be useful tools when conducting comparative analyses of behavioral data collected on animals in outdoor environments.     

Intraspecies variation in dominance style of Macaca fuscata

Knowledge of intraspecific variation is important to test the evolutionary basis of covariation in primate social systems, yet few reports have focused on it, even in the best-studied species of the Macaca genus. We conducted a comparative study of the dominance styles among three provisioned, free-ranging groups of Japanese macaques at Shodoshima Island, Takasakiyama Mountain and Shiga Heights, and collected standard data on aggressive and affiliative behavior during a period of 5 years. Our data in the Takasakiyama and Shiga groups support previous studies showing that Japanese macaques typically have despotic social relations; nevertheless, our data in the Shodoshima group are inconsistent with the norm. The social traits of Shodoshima monkeys suggested that: (1) their dominance style is neither despotic nor tolerant but is intermediate between the two traits; (2) some measures of dominance style, e.g., frequency and duration of social interactions, covary as a set of tolerant traits in Shodoshima monkeys. This study suggests broad intraspecific variation of dominance style in Japanese macaques as can be seen in some other primate species.     

Patterns and Trends in Primate Pair Bonds

Pair-bonding may be a significant feature of the social repertoire of some primate species. However, discerning inter- and intraspecific pair bonds is problematic. I present an overview of the general behavior and ecology of species reported to occur in two-adult, pair-bonded groups. There is no two-adult grouped nonhuman primate species in Africa and only two types in Asia. Behavioral and ecological data suggest that the two-adult group or pair-bonding or both may have evolved separately 4–7 times. I propose that two pair-bond components—social pair bond and sexual pair bond—occur and can be defined and described in such a manner that facilitates comparative analysis across primate taxa. The evolution of grouping patterns in many two-adult grouped primates may be best modeled via evolutionary scenarios relying on direct dietary/energetic constraints, predation, and possibly mate-guarding. There is little support for the infanticide prevention and bodyguard hypotheses of female-choice models.     

Comparative Analysis of the Macroscale Structural Connectivity in the Macaque and Human Brain

The macaque brain serves as a model for the human brain, but its suitability is challenged by unique human features, including connectivity reconfigurations, which emerged during primate evolution. We perform a quantitative comparative analysis of the whole brain macroscale structural connectivity of the two species. Our findings suggest that the human and macaque brain as a whole are similarly wired. A region-wise analysis reveals many interspecies similarities of connectivity patterns, but also lack thereof, primarily involving cingulate regions. We unravel a common structural backbone in both species involving a highly overlapping set of regions. This structural backbone, important for mediating information across the brain, seems to constitute a feature of the primate brain persevering evolution. Our findings illustrate novel evolutionary aspects at the macroscale connectivity level and offer a quantitative translational bridge between macaque and human research.     

Coevolution of vocal communication and sociality in primates

Understanding the rules that link communication and social behaviour is an essential prerequisite for discerning how a communication system as complex as human language might have evolved. The comparative method offers a powerful tool for investigating the nature of these rules, since it provides a means to examine relationships between changes in communication abilities and changes in key aspects of social behaviour over evolutionary time. Here we present empirical evidence from phylogenetically controlled analyses indicating that evolutionary increases in the size of the vocal repertoire among non-human primate species were associated with increases in both group size and time spent grooming (our measure of extent of social bonding).     

Evolution of Primate Social Systems

We review evolutionary processes and mechanisms that gave rise to the diversity of primate social systems. We define social organization, social structure and mating system as distinct components of a social system. For each component, we summarize levels and patterns of variation among primates and discuss evolutionary determinants of this variation. We conclude that conclusive explanations for a solitary life and pair-living are still lacking. We then focus on interactions among the 3 components in order to identify main targets of selection and potential constraints for social evolution. Social organization and mating system are more closely linked to each other than either one is to social structure. Further, we conclude that it is important to seek a priori measures for the effects of presumed selective factors and that the genetic contribution to social systems is still poorly examined. Finally, we examine the role of primate socio-ecology in current evolutionary biology and conclude that primates are not prominently represented because the main questions asked in behavioral ecology are often irrelevant for primate behavior. For the future, we see a rapprochement of these areas as the role of disease and life-history theory are integrated more fully into primate socio-ecology.     

Female sexual advertisement reflects resource availability in twentieth-century UK society

Evolutionary theory suggests that men and women differ in the characteristics valued in potential mates. In humans, males show a preference for physical attractiveness, whereas females seek cues that relate to resources and future earning potential. If women pursue marriage as an economic strategy, female sexual advertisement should increase during periods of poor economic conditions when the number of high-quality male partners becomes a limited resource. To test this prediction, measures of skin display and clothing tightness were taken for clothes portrayed in UK Vogue magazine from 1916 to 1999. These estimates of sexual advertisement were analyzed in relation to an index of economic prosperity (GDP), while controlling for general increases in economic conditions and sexual display over the course of the past century. The results indicate that female sexual display increases as economic conditions decline, with the level of breast display and the tightness of clothing at the waist and hips the key factors underlying this increase. Breast size and symmetry and female body form are secondary sexual characteristics that play an important role in sexual attractiveness. Since advertisement of these features increases as levels of competition for high-quality partners increases, females appear to use marriage as an economic strategy. Patterns of female fashion appear to be underpinned by evolutionary considerations relating resource availability to female reproductive success. Russell Hill, B.Sc., M.Phil., Ph.D. is an Addison Wheeler Research Fellow at the University of Durham. His main research interests are in the evolution of mammalian social systems and his current projects span evolutionary anthropology, conservation biology, and theoretical modeling. Sophie Donovan B.Sc., M.Sc. has recently completed an M.Sc. in Speech and Language Sciences at University College London, focusing on the development of a deaf child’s vocabulary through conversations in the classroom. She is currently practicing as a Speech and Language Therapist. Nicola Koyama, B.Sc., Ph.D. is a Senior Lecturer at Liverpool John Moores University. Her principal research interests lie in the evolution of social systems in human and non-human primates, in particular the regulation of social relationships, mate preferences, and conflict management.     

Brain reorganization,not relative brain size,primarily characterizes anthropoid brain evolution

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.     

Olfactory evolution and behavioral ecology in primates

Primates are usually thought of as "visual" mammals, and several comparative studies have emphasized the role of vision in primate neural and sociocognitive specialization. Here I explore the role of olfactory systems, using phylogenetic analysis of comparative volumetric data. The relative sizes of the main olfactory bulb (MOB) and accessory olfactory bulb (AOB) tend to show different evolutionary patterns in accordance with their different functions. Although there is some evidence of correlated evolution of the two systems, this is apparent in only one clade (the strepsirhines). As predicted, the MOBs correlate predominantly with ecological factors (activity period and diet), while the AOBs correlate with social and mating systems. Related olfactory structures (i.e., the piriform cortex and amygdala) exhibit correlated evolution with the AOBs but not with the MOBs, and the corticobasolateral part of the amygdala exhibits a correlation with social group size in platyrrhines similar to that observed for the AOB. These social system correlations support the idea that there is an olfactory dimension to the concept of the social brain.     

Primate home range and GRIN2A, a receptor gene involved in neuronal plasticity: implications for the evolution of spatial memory

N -methyl- d -aspartate (NMDA) glutamate receptors play crucial roles in neuronal synaptic plasticity, learning and memory. However, as to whether different NMDA subunits are implicated in specific forms of memory is unclear. Moreover, nothing is known about the interspecific genetic variability of the GRIN2A subunit and how this variation can potentially explain evolutionary changes in behavioral phenotypes. Here, we used 28 primate GRIN2A sequences and various proxies of memory across primates to investigate the role of GRIN2A . Codon-specific sequence analysis on these sequences showed that GRIN2A in primates coevolved with a likely ecological proxy of spatial memory (relative home-range size) but not with other indices of non-spatial learning and memory such as social memory and social learning. Models based on gene averages failed to detect positive selection in primate branches with major changes in relative home-range size. This implies that accelerated evolution is concentrated in specific parts of the protein expressed by GRIN2A . Overall, our molecular evolution study, the first on GRIN2A , supports the notion that different NMDA subunits may play a role in specific forms of memory and that phenotypic diversity along with genetic evolution can be used to investigate the link between genes and behavior across evolutionary time.     

Primate brain evolution: Integrating comparative,neurophysiological, and ethological data

“Undoubtedly the most distinctive trait of the Primates, wherein this order contrasts with all other mammalian orders in its evolutionary history, is the tendency towards the development of a brain which is large in proportion to the total body weight, and which is particularly characterized by a relatively extensive and often richly convoluted cerebral cortex (p. 228).” 1 While this statement is generally true, primate brains vary in size nearly one thousand‐fold, from a mass of 1.8 g in the tiny mouse lemur to 1,300 g in modern humans. Many attempts have been made to understand both the distinctiveness of primate brains and the variation observed within the order: How did such variation evolve and why, and what are its cognitive implications? Following Jerison's 2 masterly review thirty years ago, comparative studies have highlighted suggestive correlations of brain size. However, the meaning and validity of these correlations have been vigorously debated. It has become clear that progress depends on taking great care in the use of comparative methods and in finding multiple converging strands of comparative evidence as opposed to making speculative interpretations of single correlations. In particular, recent work demonstrates the value of examining how evolutionary changes at different anatomical levels interrelate.